Joaquin Caro-Astorga1
Joseph T. Meyerowitz1
Devon A. Stork2
Una Nattermann2
Samantha Piszkiewicz3
Lara Vimercati4
Petra Schwendner5
Antoine Hocher6
Charles Cockell7
Erika DeBenedictis1,2*- 1The Francis Crick Institute, London, United Kingdom
- 2Pioneer Research Laboratories, San Francisco, CA, United States
- 3Pivot Bio, Berkeley, CA, United States
- 4Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, United States
- 5University of Florida, Gainesville, FL, United States
- 6London Institute of Medical Sciences, London, United Kingdom
- 7UK Centre for Astrobiology, University of Edinburgh, Edinburgh, United Kingdom
Nature exhibits an enormous diversity of organisms that thrive in extreme environments. From snow algae that reproduce at sub-zero temperatures to radiotrophic fungi that thrive in nuclear radiation at Chernobyl, extreme organisms raise many questions about the limits of life. Is there any environment where life could not “find a way”? Although many individual extremophilic organisms have been identified and studied, there remain outstanding questions about the limits of life and the extent to which extreme properties can be enhanced, combined or transferred to new organisms. In this review, we compile the current knowledge on the bioengineering of extremophile microbes. We summarize what is known about the basic mechanisms of extreme adaptations, compile synthetic biology’s efforts to engineer extremophile organisms beyond what is found in nature, and highlight which adaptations can be combined. The basic science of extremophiles can be applied to engineered organisms tailored to specific biomanufacturing needs, such as growth in high temperatures or in the presence of unusual solvents.
Introduction
Extremophilic microbes have long been studied in hopes of better understanding the origin and limits of life. Extremophile biology is also relevant to biomanufacturing (Ye et al., 2023), where large-scale growth occurs in non-natural, extreme chemical conditions ranging from the use of toxic waste streams as feedstocks to the intentional production of toxic chemicals like butane. The space science community hopes to push the capabilities of biomanufacturing even further for in situ resource utilization (ISRU) (Cockell, 2022), especially on human missions to the moon, Mars, and beyond. This will require microbes that are well adapted to chemically unusual feedstocks derived in part from highly oxidized Moon regolith or perchlorate-containing Mars regolith. A microbe that can thrive, growing and metabolizing at high rates, in extreme bioprocessing conditions can enable robust, high-yield, and low-cost synthesis of biological products. We aim to not just understand the basic science of extremophile biology, but also how that basic science supports current and future extremophilic bioengineering.
Precedent for bioengineering extremophilic traits
Extremophilic tools and traits can be engineered in two ways. Individual extremophilic enzymes such as thermostable amylases, cold-adapted β-glucosidases, DNA-dependent DNA polymerases, and high pH tolerant lipases enable extremophilic catalysis abilities for varied uses (Chien et al., 1976; Zhu et al., 2020). Whole extremophile organisms, including engineered strains, are used to produce ectoine, polyhydroxyalkanoate, polyhydroxybutyrate, and other bioproducts (Tan et al., 2011; Chavan et al., 2021; Hu et al., 2024). Growth in extreme environments also enables new kinds of fermentation, such as non-sterile continuous production in seawater, and gas fermentation in waste gasses from steel production (Yue et al., 2014; Molitor et al., 2016). Biomanufacturing in terrestrial or space processes will require advances in basic fermentation approaches. Desirable extremophilic traits such as tolerance to potentially toxic waste-derived feedstocks, growth in extreme environments hostile to contaminants, and desiccation tolerance open access to entirely new types of bioproduction processes (Chen and Jiang, 2018; Averesch et al., 2023).
The table below summarizes the current understanding of how each category of extremophile adaptation works, and whether there is precedent for deliberately endowing a new organism with this adaptation through bioengineering (Table 1). Growth of microorganisms in some extremes, such as low or high temperature and high radiation, have been comprehensively explored, and are mechanistically quite well understood. Other extremes require more complex equipment to simulate, most notably altered gravity and high and low pressure. This presents a substantial barrier for experimentation. For these extremes, initial studies have been completed, but more research is needed to replicate and interpret results.
Table 1. Precedent for bioengineering extremophilic traits.
Low gravity is an especially challenging extreme to study due to the cost and technical complexity of conducting experiments. Low gravity eliminates convection, which may substantially alter the function of microorganisms in ways that may be difficult to simulate on the ground. Low gravity simulation devices can prevent sedimentation but do not eliminate convection (Vroom et al., 2022), and it remains unknown the extent to which these devices are a good proxy for low gravity microbial growth. To reliably investigate low gravity conditions, experiments must be done on experimental platforms in space, such as in Low Earth Orbit.
Low atmospheric pressure would similarly benefit from further research. One paper adapts Bacillus subtilis to grow better in liquid culture exposed to low-pressure atmospheric conditions (Nicholson et al., 2010). However, it is unclear whether the experimental setup for this study selects for ‘growth at low pressure’ or simply growth in less well-aerated media. Analysis of the accumulated mutations suggests evolution was driven by the particular experimental conditions rather than low pressure. Mutations in rnjB, an RNAse, improves growth at 27°C regardless of air pressure (Waters et al., 2015), and can be interpreted as an adaptation of B. subtilis for low temperature. The rnjB mutation could account for most of the fitness gain, although additional mutations were also observed (Waters et al., 2021) impacting membrane fluidity and the regulation of anaerobic metabolism such as increased expression of nitrate reductases. Studies of organisms growing on solid media under low pressure may clarify some of these issues.
Tolerance to extremes can be engineered by directly transferring specific genes that improve microbes performance. For example, the transfer of the carrot gene hps17.7 to Saccharomyces cerevisiae improved both growth rate and maximum culture density under low temperature (25°C) and acidic conditions (pH 4) plus high osmolarity (0.8 M sorbitol). Percentage of survival at 47°C increased from 15% of the wild type to 38% of the engineered strain (Ko et al., 2017). This is one of the examples where genetic parts from one species can improve survival for another.
Thrive versus survive
When we envision using extremophiles for biomanufacturing, we require microbes that are capable of rapidly producing biomass under extreme conditions, not just surviving in a dormant state. The literature often conflates the ability to survive temporary exposure to extreme conditions with the ability to thrive and reproduce. Here, we explore the known limits of five well-studied extremophilic organisms; Bacillus subtilis, Deinococcus radiodurans, Thermus aquaticus, Psycromonas ingrahaii, and Thermus thermophilus; and their ability to thrive and survive in extreme environments (Figure 1, references in Supplementary Table S1). Engineered extremophiles should be measured against two separate benchmarks: their ability to thrive in an extreme environment (divide under extreme conditions) and separately their ability to survive (tolerate and reproduce after temporary exposure to even more extreme conditions). A specific example of this distinction can be seen between related alkalophilic and alkaline-tolerant Bacillus spp. (Guffanti et al., 1980). These strains differ in pH homeostatic mechanisms and growth pH range, though their cytoplasmic pH ranges share a common alkaline limit.
Figure 1. Microbes can survive conditions too extreme for growth. A visualization of the thriving and survival limits of organisms. For a list of citations for each organism in each condition, see Table S1. Graphs indicate the limits of thriving and survival in extreme conditions of temperature, pH, and salinity (% NaCl) for each of the five organisms.
Some organisms are capable of entering dormant states, becoming unable to replicate, but even more capable of surviving extreme conditions. For example, Bacillus experiences sporulation in which a copy of the genome to be encased in a metabolically inactive and well protected desiccated spore. When favorable conditions return, the spore can germinate, shedding its protective layers and initiating the formation of a new vegetative cell through the reactivation of essential cellular processes (McKenney et al., 2013). Organisms when in sporulated form can survive even more extreme conditions than their non-supported equivalents (Cho and Chung, 2020).
Somatic adaption versus genetic mutation
The extremophile literature often focuses on genome-level changes as the primary drivers of extremophilic properties. However, simply modulating the expression of endogenous genes is a more subtle yet equally profound aspect of the survival strategy of extremophiles. The dynamic nature of gene expression allows organisms to swiftly react to their environment, mounting an immediate defense against stressors without the long-term commitments tied to genetic mutations or new gene acquisition. For example, heavy water (D2O) stress in a variety of organisms is most consistent with adaptation being driven by changes in gene expression, rather than by genomic mutations (Katz and Crespi, 1966), and heterologous expression of a Deinococcus radiodurans transcriptional regulator alone can improve varied stress tolerances in multiple species (Wang et al., 2020). Extremophile bioengineering studies should separately characterize the contribution of gene reregulation, and the contribution of genome-level changes.
The root cause of stress in extreme conditions
In order to flourish, the cell must perform many essential functions, such as maintaining appropriate redox balance, membrane fluidity, protein stability balance, and limiting damage to DNA and proteins (Figure 2A). Studies of model microbes like E. coli and B. subtilus as well as non-model microbes like Lactobacillus delbrueckii and Acidithiobacillus ferrooxidans have begun to isolate the proximal mechanism by which extreme conditions disrupt these essential functions (Table 2). There are four broad classes of proximal cases of stress in extreme conditions: generation of reactive oxygen species (ROS), damaging DNA or proteins in ways that break or form chemical bonds, destabilizing the fold of a protein in ways that do not break chemical bonds, and altering the fluidity of the cell membrane. Different stressors most directly impact one or several of these proximal causes of stress. For example, high temperature directly destabilizes folded proteins and increases the error rate during DNA replication (Velichko et al., 2012).
Figure 2. Root causes of stress under extreme conditions. There are several essential cellular functions that are frequently the proximal cause of disruption in extreme conditions (A). When an essential function is disrupted, it can lead to disruption of other essential functions, resulting in a cascade of failure (B). Resistance mechanisms can protect against multiple extremes with the same root cause (C), and stressors with opposite root causes can be easier to tolerate together than separately (D).
Table 2. Direct effects of extreme conditions.
In addition to direct disruption of important cellular functions, breakdown of one function can lead to a further cascade of failures, such as unfolded DNA repair proteins further increasing the effective DNA replication error rate (Figure 2B). Understanding the root cause of stress in extreme conditions can allow us to reason about which polyextremophiles are biophysically realistic, and which adaptations they might possess. Organisms can tolerate multiple extremes at once if those extremes have the same root cause and thus a similar tolerance mechanism (Figure 2C), for example, the same genes enhance tolerance to both perchlorate and UV radiation in E. coli (Lamprecht-Grandío et al., 2020). For example: perchlorate tolerance and high radiation tolerance are both enabled by improved DNA and protein protection and repair (Slade and Radman, 2011; Lamprecht-Grandío et al., 2020). Freezing environment threats comprise crystals formation and local/temporal solute concentration. Similarly, salt tolerance and freeze–thaw tolerance can be synergistic: a metagenomic study of organisms from brines and alkaline lakes found that these salt-tolerant microbes are also 1,000-fold more resistant to freeze–thaw due to high intracellular levels of osmolytes and biofilm formation (Wilson et al., 2012). Conversely, some combinations of extremes are easier to tolerate together than separately because they exert opposing root causes (Figure 2D). High temperature is easier to tolerate in the presence of kosmotropic salts such as NaCl (Chin et al., 2010). Low temperature is easier to tolerate in the presence of chaotropic salts such as MgCl2 (Hallsworth et al., 2007; Chin et al., 2010). Haloalkaliphiles demonstrate adaptations to combined stresses (Wiegel and Kevbrin, 2004; Mesbah and Wiegel, 2012) and apparent trade-offs between adaptation to each separate stress (Mesbah and Wiegel, 2011; Banciu and Muntyan, 2015).
However, more research is needed into the mechanism of action of different stress adaptations. Not all extremophile organisms exhibit correlation between growth in multiple extremes that would be expected from Table 2. Early studies showed the D. radiodurans stress response to ionizing radiation shares mechanisms with desiccation response, suggesting adaptation to desiccation causes radiation tolerance (Shukla et al., 2007; Ujaoney et al., 2017). Later studies show desiccation stress and radiation tolerance are not correlated in anaerobes, while presence of certain manganese complexes was predictive of radiation tolerance across bacteria, fungi, archaea, and eukarya (Daly, 2009; Sharma et al., 2017; Beblo-Vranesevic et al., 2018). It is unknown how many different adaptations may be used to cope with a particular combination of extremes, if any. For example, there are no known microbes that grow robustly at extreme high and low pH (Jin and Kirk, 2018) or at extreme high and low temperature (Wiegel, 1990), though some organisms are claimed to tolerate ranges of 10 pH units and 60°C (Pandey et al., 2014). This may demonstrate a fundamental limit for microbial metabolism, or it may be a reflection of evolution in environments with limited variation in pH and temperature. Knowledge of compatibility, trade-offs, and relative efficiency between known adaptations will improve design and bioengineering of microbes with extremophilic traits.
Approaches for polyextremophile bioengineering
There are several approaches to engineer or enhance extreme properties in microbes depending on the type of stress to be addressed and the amount of prior knowledge about tolerance mechanisms. Biocontainment is an overarching consideration when engaging with an extremophile engineering campaign to prevent the release and uncontrolled spread of genetically engineered organisms. Rational design requires adding exogenous DNA with a known function, such as the tardigrade Dsup DNA repair gene which enhances survival by 2 orders of magnitude when transferred to E. coli grown in harsh conditions (Puig et al., 2021). Knowledge of specific extremophilic genes like tardigrade Dsup, as well as genome-scale models such as flux balance analysis (Noirungsee et al., 2024; Saldivar et al., 2024), can both be invaluable for engineering (Swayambhu et al., 2020). If there are no known genes with the needed function, metagenomic libraries sourced from extreme environments can search for genes that confer protection without foreknowledge of the sequence-function relationships (Biver et al., 2014; Culligan et al., 2014; Forsberg et al., 2016; Ausec et al., 2017).
With or without rational genetic engineering, directed evolution can be applied to improve desired properties. In directed evolution, where a library of variants from a starting organism are made, fitness is measured, and improved variants are used as the starting point for iterative rounds of improvement. In cases where an organism’s ability to grow in new extreme conditions is the evolutionary goal, the process is called adaptive lab evolution (Mavrommati et al., 2022). Changes across the whole proteome, not just a single protein or pathway, are required for global adaptations to multi-target stresses (Fernandes et al., 2023) such as high temperature (Deatherage et al., 2017), high salinity (Dhar et al., 2011), and high oxidative stress (Papiran and Hamedi, 2021). Some metabolic adaptations such as improved growth on alternative carbon sources (Chen et al., 2020; Espinosa et al., 2020) or efficient photosynthesis in high light (Dann et al., 2021) have been demonstrated, each requiring tens to hundreds of mutations. These adaptations can produce trade-offs, where fitness in the original growth conditions or resistance to other extremes is reduced (Caspeta and Nielsen, 2015; Cheung et al., 2021). Alternating selective conditions, such as switching between high and low temperature between growths, can produce different adaptations than selection in constant conditions (Lambros et al., 2021; Carpenter et al., 2023). Some trade-offs may be a reflection of the chosen selective conditions, not an underlying innate limit of biology.
Extremophile engineering can combine strategies logically (Figure 3). If there are known genes with known functions conferring resistance to the target extreme condition, they can be used as a starting point for engineering and directed evolution. If no usable sequence-function relationships are known, metagenomic screens and functional genomics can discover new genes with the desired function (Mirete et al., 2016). Adaptive laboratory evolution can be used to further integrate, refine and evolve the transferred genes within the original genome, adjusting molecular interactions, protein stability, expression levels, burden, etc.
Figure 3. Polyextremophiles bioengineering approaches. This graph sketches the current approaches taken to evolve microorganisms, which can be combined in series to maximize the resilience achieved.
Conclusion
Our consistently improving understanding of extremophiles and their mechanisms of adaptation, together, provide new opportunities to actively engineer new extremophilic capabilities. Today, extremophile properties that are simple to simulate in the lab (especially high temperature tolerance, radiation tolerance, and salt tolerance) are thoroughly studied, well mechanistically understood, and the ability to deliberately engineer these properties in target microbes has been explored. To expand our capacity to engineer biology, scientists need new tools to identify and culture unusual extremophile microbes under stringent growth conditions, such as high pressure or low gravity. Climate scientists and the biomanufacturing industry can provide the essential insights to identify the best opportunities for the engineering of extreme biology. As the field shifts to focus toward bioengineering, so too will the vocabulary — the reporting for studies must focus more directly on measuring rates of biomass or protein production under extreme conditions, rather than simply reporting binary survival or death.
Unanswered questions remain about the extent to which extremophile properties can be combined, enhanced, or transferred to new microbes. Today, we know enough about the root causes of stress under extreme conditions to deliberately equip microbes with adaptations that are likely to enhance performance in a new extreme environment. However, natural organisms continue to surprise us with new mechanisms for adaptation, making it valuable to continue to sample and study new wildtype organisms from extreme environments. Further study into the fundamental limits of life, and new methods for systematic probes of these limits, will allow us to engineer custom microbes designed to thrive in the exotic, artificial niches encountered in the future.
Author contributions
JCA: Writing – original draft, Writing – review & editing. JM: Writing – review & editing. DS: Writing – review & editing. UN: Writing – review & editing. SP: Writing – review & editing. LV: Writing – review & editing. PS: Writing – review & editing. AH: Writing – review & editing. CC: Writing – review & editing. ED: Writing – original draft, Writing – review & editing.
Funding
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. JCA, JM, and ED were supported by the Francis Crick Institute which receives its core funding from Cancer Research UK (CC2239), the UK Medical Research Council (CC2239), and the Wellcome Trust (CC2239), and a Steel Perlot Early Investigator Grant. DS, UN and ED are supported by funding from The Astera Institute. AH is supported by Medical Research Council core funding (MC-A658-5TY40).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmicb.2024.1341701/full#supplementary-material
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Keywords: extremophile, directed evolution, functional genomics, ISRU, biomanufacturing
Citation: Caro-Astorga J, Meyerowitz JT, Stork DA, Nattermann U, Piszkiewicz S, Vimercati L, Schwendner P, Hocher A, Cockell C and DeBenedictis E (2024) Polyextremophile engineering: a review of organisms that push the limits of life. Front. Microbiol. 15:1341701. doi: 10.3389/fmicb.2024.1341701
Edited by:
Mohamed Jebbar, Université de Bretagne Occidentale, FranceReviewed by:
Francesco Venice, National Research Council (CNR), ItalyNancy Merino, Lawrence Livermore National Laboratory (DOE), United States
Copyright © 2024 Caro-Astorga, Meyerowitz, Stork, Nattermann, Piszkiewicz, Vimercati, Schwendner, Hocher, Cockell and DeBenedictis. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Erika DeBenedictis, ZXJpa2FAcGlvbmVlci1sYWJzLm9yZw==